THE TEMPERATURE CHARACTERISTIC FOR PHARYNGEAL BREATHING RHYTHM OF THE FROG Academic research paper on "Art (arts, history of arts, performing arts, music)"

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By W. J. CROZIER* and T. B. STIER. {From the Zoological Laboratory, Rutgers University, New Brunswick)

(Accepted for publication, January 26, 1925.) I.

Published observations upon metabolism of frogs as a function of temperature suffice to indicate that a zone of temperature exists in the o

neighborhood of 15°C. which is a kind of critical temperature, in the sense that there the curve relating temperature to velocity of vital d

may appear the practical independence of the speed of gaseous ex- o

change and the temperature, between 15° ± and 20° ± (Vernon, 3

1897; Jones, 1923). This independence has been interpreted to signify p

capacity of the frog to regulate its own metabolism, independently of environmental temperature, within a certain range. We shall point out that this conclusion may not be altogether necessary, or correct. .

For a number of other instances, including activities of organs and (g

tissues of frogs, it has been shown that at about 150 there may occur a o

sharp change in the relationship between temperature and the veloci- ;>

ties of protoplasmic activities (Crozier, 1924-25, a, b; Crozier and Pilz, 1924; Crozier and Federighi, 1924r-25, a; Glaser, 1924-25), and that among the several expressions of such effects (Crozier 1924-25, a; Crozier and Stier, 1924-25) there may be found, at about 15°C. relatively enhanced variability in the biological result, or a zone of very slight average change in the temperature relation. Unpublished experiments with the ciliated epithelium of frog esophagus show a similar change in the curve of relation between ciliary activity and temperature. We desired to see, therefore, if the supposed autonomous control of the frog's metabolic processes within an interme* Research Associate, Carnegie Institution of Washington.

The Journal of General Physiology

diate range of temperatures might not find its explanation in terms of such observations.

For this purpose, in part, we have studied the pharyngeal breathing rhythm. It will be shown that there does exist a small intermediate range of temperatures in which the frequency of the pharyngeal rhythm of frogs may seem independent of temperature; we believe that the explanation is in large part to be given through the conception of interconnected processes determining the breathing rhythm.

A further reason for the study of pharyngeal rhythm in the frog lies in the opportunity for partially testing one view as to the control of the activity of the medullary respiratory center. According to Winterstein (1911) and others, hydrogen ion may be the respiratory hormone. If the frequency of pharyngeal movements were determined through some event catalyzed by H+, it might be expected that the critical thermal increment for this rhythm would correspond with that for known H+-catalyzed processes (i.e., about 20,000 calories). The experiments fail to support the notion of direct cataly-

sis by H+, and in this agree with (unpublished) experiments upon m

fishes; but beyond this they do not permit more than a suggestion as to g

the nature of the controlling process. The movements involved are uu

pharyngeal movements, serving merely to renew air within the buccal r

cavity and during which the glottis is closed, not proper movements s

of lung ventilation (Baglioni, 1900; 1911), although presumably °

innervated from the respiratory center (for review of innervation, °

cf. Black, 1917). The flank movements, indicating lung filling, seem, A

however, to follow the same curve as do the pharyngeal movements— i

so far as our observations extend. The question may also be com- ,

plicated by the role of skin respiration; in this respect the frog as a 0

test object is perhaps inferior to the insects we have studied previously (Crozier and Stier, 1924-25).

In measuring the pharyngeal rhythm of frogs (Rana pipiens) each individual, previously adapted during 4 to 35 days to ordinary room temperature, was placed in a 500 cc. bottle immersed in a large jar of water of which the temperature was under control. Through the totally immersed bottle was drawn a continuous current of mois-


tened air previously brought to thermostat temperature by passage through a coil of tubing in the water. A sensitive thermometer graduated to 0.1° had its bulb adjusted near the frog's head. In a few experiments the air was changed intermittently. If the thermostat be surrounded with yellow paper, feebly illuminated by indirect light, the frog maintains an almost constant position for hours. Movements of the pharyngeal floor are then easily observed through a small window in the jacket of the thermostat. The absence of spontaneous movements, thus largely insured by removing the likelihood of visual stimulation, is extremely important for significant measurements of respiratory frequency. The illumination, of itself, does not materially influence the pharyngeal rhythm (Crofts and Laurens, 1924).

as previously noted for breathing movements of insects (Crozier and l

Stier, 1924-25). As a rule the shallow movements at the beginning §

of a breathing cycle are slower than the deeper movements at its d

close, leading up to lung inflation, but this correlation may be reversed. r

constant temperature, the time for ten movements being obtained at g

each observation. The plotted points are averages of such series. The temperature was changed by small steps. After each such

change, at least 10 minutes ss

1912) (or nares?), and should give a delicate method for its investi- ,

gation. 0

Each experiment consisted in obtaining a series of readings with a 5

single animal over a convenient range of temperatures. Eighteen winter individuals, weighing 20 to 30 gm, each, were thus studied. Within two thermal regions respectively above and below 15° ± the effects of warming or of cooling are quickly reversible. But if one attempts to pass quickly from, say, 18° to8°, complications may appear. In the light of experiments designed to test the mechanism of thermal adaptation it seems to us probable that these complications will prove useful in analyzing the basis of long-period adaptation to particular temperatures. Our purpose now, however, is merely to

obtain significant values of the temperature characteristic for pharyngeal rhythm, and discussion of adaptation is postponed.

The result of a single typical experiment is given in Fig. 1. The possible working range is from about 6-28° or less. It is clear that in the vicinity of 15° there occurs a change in the effect of temperature. The expression of this change is somewhat different from that observed in a number of other cases (Crozier, 1924-25, b). For the latter,

involving an unmistakable shift in the slope of the log V — ^ line,

the explanation was advanced that on either side of 15° ± a different

the slow process determining the velocity of the whole. It should be |

clear that this type of explanation, for which there is indication of §

experimental support (Crozier and Stier, 1924-25), need not prevent d

the recognition of other kinds of temperature effects. Thus it might r

be supposed that the velocity of a given vital process is determined |

particular range of temperatures the effective amount of this material could not be brought to exceed a certain maximum quantity. There is evidence for the occurrence of such cases, in which we may assume S

that the significant material, X, or a precursor of it, accumulates as r

change should occur in the structure of the surface, it may remain A

saturated with X over a wide range of temperature; and the velocity l

of the dependent process correspondingly remain sensibly constant. ,

While this conception may prove useful, it may not be necessary. 0

The peculiar course of the curve in Fig. 1 may be due in part to that 5

averaging of the effects of competing processes which is implicit in the taking of the observations. This is particularly true because the temperature 15° ± 1° is a region where, even in spite of careful shielding from visual and other disturbance, the frog tends to exhibit one or more spontaneous jumps, or sudden changes of position. For example, if the animal be very slowly cooled (0.1° per 10 minutes) from, say, 23°, it is motionless until approximately 15° is reached. By the time 14° is reached the frog is quiet again, and may so continue


for as much as 8 hours. This trigger effect is very curious, but we believe it comprehensible in terms of the theory already discussed (Crozier, 1924—25, a, b; Crozier and Federighi, 1924-25, a; Crozier and Stier, 1924r-25). When muscular movements occur, the frequency


- O*??*® ^d //»8,600

_ No. 17c? I

000345 0.00355


Fig. 1. Observations with Frog 17, illustrating characteristic break in the temperature effect. Each point is the mean of a series of observations at constant temperature.

24 &23

J 1.9 L8

"®<2L ,/? Ja-S^ ve -

- -a mX /U" 8,700

1 15° * A ^^


0.0035 1/T8abs.


Fig. 2. Experiments with frogs not adjusted to laboratory temperature (cf. text); the data for one animal have been multiplied by 2.9 in order to bring them into the field of the remaining (unadjusted) observations.

of pharyngeal rhythm is increased. Consequently there appears a distinct bump on some curves such as are shown in Fig. 2.

It may be emphasized that if the breathing rhythm were to be studied from the usual standpoint of temperature coefficients (Qw ratio), these types of irregularity could scarcely be dealt with, and

Qi Q. CD Q.

CD in .

would indeed probably escape detection altogether. Effects of the sort illustrated in Fig. 1, and subsequent figures, are scarcely explicable by the assumption that the frog is able to control its body temperature, within a certain zone of external temperatures near 15°.

To obtain a working interpretation of the temperature effect a larger array of data is required. Fig. 2 contains the records from several frogs of similar size and antecedents, which were under laboratory conditions for less than 2\ days—previously having been exposed to low temperatures approximating that out-of-doors {i.e.,

for the lower range of temperatures (6-15° ±) is ¡j, — 8,700. Fig. 3 o

contains similar records for frogs adapted for 4 to 39 days to ordinary e

laboratory temperature; here n = 8,830. The figures for breathing r

frequency are less concordant among the different individuals than is |

the case for those not adjusted to laboratory temperatures, but the g

13°, while with the non-adjusted animals the frequency is sensibly S

increment from combined data. The value thus secured agrees with 3

ences are in part traceable to the extent of intrinsic variation in breath- ,

ing frequency, and thus to the difficulty of obtaining a good fitting 2

line when the slope (Figs. 2 and 3) is slight; the low rate of change with changing temperature, moreover, tends to magnify errors of timing.

A critical increment agreeing sufficiently well with that obtained for Rana pipiens has been deduced from the breathing rhythm of the bull-frog {Rana catesbiana). Two sets of observations are plotted in Fig. 4.

From the standpoint employed in previous papers this result is taken to mean that the frequency of breathing movements is governed by a reaction which controls the velocity of production of a deter-


mining substance. The critical increment characteristic of this reaction appears to belong among the group of those associated with energy-providing processes in protoplasm (Crozier, 1924-25, b; Crozier and Stier, 1924-25).


0.0035 1/T°ab5.


Fig. 3. Experiments with frogs adapted to laboratory temperature for 4 to 39 days. The averages from each animal are multiplied by a specific factor, to facilitate comparison.

_ —Q^ // = 7,100±

•No 16$ o No! Z $





Fig. 4. Experiments with two bull-frogs {Rana catesbiana).

Oí Q. cd q.

cd in .

To make the picture definite, let it be supposed that the frequency of the respiratory movements depends upon synaptic activities; for - example, upon the frequency with which the synaptic galaxy in the respiratory center acts as an open valve, permitting escape of im-

pulses constantly generated within internunical neurones of the respiratory center. The open state of the valve is then taken to be a function of reactions occurring in the synapse. The velocity with which molecules of the effective substance are produced may conceivably be caused to differ in several ways on either side of a recognizably critical temperature. The linked processes producing it may be differentially affected by change of temperature to such extent that a new reaction becomes the slow process, imposing its particular increment upon the whole; or at a certain temperature the concentration of the mother-substance generating active catalytic molecules for this reaction may be decreased through some physical change in the protoplasm. The latter result would produce an abrupt change in the velocity of the

end-result, but without changing the critical increment (cf. Fig. 1). °

It is of course possible that both these effects should occur simultane- |

ously; or if not quite simultaneously, that their independent occur- g

rences should contribute to irregularity in the vicinity of, say, 15° ±. e

Inspection of the plottings in Figs. 2 and 3 shows that in some cases the frequency of movements at temperatures above 15° falls consistently above the line derived from observations below 15°, rather g than that the physical basis of the shift is irreversible. We may speak of physical alterations in the protoplasm (surface films ?) as determining abrupt changes, yet not progressively influencing the velocity s of vital activities in relation to temperature, because one obtains o satisfactory agreements with the Arrhenius equation; hence diffusion ° effects may be neglected.

The assumption of synaptic location for the processes governing breathing frequency is made because the critical increment agrees ,

with that deduced for synaptic delay and for some related phenomena 0

in amphibians. 5


The frequency of the pharyngeal respiratory rhythm of frogs exhibits a critical thermal increment p = 8,800 calories. At about 15° irregularities are apparent, which may be reduced by continued adaptation to room conditions. The frequency depends upon a process possibly synaptic in locus and apparently belonging among the


group of respiratory reactions. Its temperature characteristic sharply separates this process from those reactions known to be catalyzed by H ion.


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Baglioni, S., 1900, Arch. Anat. u. Physiol., suppl. 33; 1911, Ergebn. Physiol., xi, 531.

Black, D., 1917, J. Comp. Neurol, xxviii, 379. Crofts, E. E., and Laurens, H., 1924, Am. J. Physiol., lxx, 300. Crozier, W. J., 1924-25, a, J. Gen. Physiol., vii, 123; 1924-25, b, J. Gen. Physiol., vii, 189. Crozier, W. J., and Pilz, G. F„ 1923-24, J. Gen. Physiol., vi, 711.

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